Histone acetyltransferase GCN5 contributes to cell wall integrity and salt stress tolerance by altering the expression of cellulose synthesis genes

Abstract

Summary Excess soluble salts in soil are harmful to the growth and development of most plants. Evidence is emerging that the plant cell wall is involved in sensing and responding to salt stress, but the underlying mechanisms are not well understood. We reveal that the histone acetyltransferase General control non‐repressed protein 5 (GCN5) is required for the maintenance of cell wall integrity and salt stress tolerance. The levels of GCN5 mRNA are increased in response to salt stress. The gcn5 mutants exhibited severe growth inhibition and defects in cell wall integrity under salt stress conditions. Combining RNA sequencing and chromatin immunoprecipitation assays, we identified the chitinase‐like gene CTL1, polygalacturonase involved in expansion‐3 (PGX3) and MYB domain protein‐54 (MYB54) as direct targets of GCN5. Acetylation of H3K9 and H3K14 mediated by GCN5 is associated with activation of CTL1, PGX3 and MYB54 under salt stress. Moreover, constitutive expression of CTL1 in the gcn5 mutant restores salt tolerance and cell wall integrity. In addition, the expression of the wheat TaGCN5 gene in Arabidopsis gcn5 mutant plants complemented the salt tolerance and cell wall integrity phenotypes, suggesting that GCN5‐mediated salt tolerance is conserved between Arabidopsis and wheat. Taken together, our data indicate that GCN5 plays a key role in the preservation of salt tolerance via versatile regulation in plants.

Insight into the Role of Epigenetic Processes in Abiotic and Biotic Stress Response in Wheat and Barley

“…The first HMT recruiters in Arabidopsis are the members of the BBR/BPC family, that were shown to be responsible for establishing the silencing mark [67,68]. As another common type of histone modification-histone acetylation-is reversible and dynamically maintained by the antagonistic action of histone acetyltransferases (HATs) and histone deacetylases (HDACs) [56,69]. It is generally realized that the acetylation neutralizes the positive charge of lysine side chains on histones and reduces its interaction with the negatively charged DNA backbone, and thus relax the chromatin structure and promote gene transcription [70,71].…”

“…Previous studies revealed that various HATs and HDACs modulate plant gene expression in response to environmental stresses in wheat and barley. For instance, TaGCN5, a wheat ortholog of Arabidopsis histone acetyltransferases AtGCN5, plays an important role in regulating wheat defense response to heat and salt stresses (Table 1) [56,57]. The expression of TaGCN5 was induced by treatment with heat and salt in bread wheat (Table 1) [56,57].…”

“…For instance, TaGCN5, a wheat ortholog of Arabidopsis histone acetyltransferases AtGCN5, plays an important role in regulating wheat defense response to heat and salt stresses (Table 1) [56,57]. The expression of TaGCN5 was induced by treatment with heat and salt in bread wheat (Table 1) [56,57]. In Arabidopsis, GCN5 protein is recruited to the promoters of HSFA3 and UVH6 (UV-HYPERSENSITIVE 6) in response to heat stress, and enriched at the promoters of CTL1, PGX3 and MYB54 (involved in tolerance of salt stress) under salt stress as well [56,57].…”

“…The expression of TaGCN5 was induced by treatment with heat and salt in bread wheat (Table 1) [56,57]. In Arabidopsis, GCN5 protein is recruited to the promoters of HSFA3 and UVH6 (UV-HYPERSENSITIVE 6) in response to heat stress, and enriched at the promoters of CTL1, PGX3 and MYB54 (involved in tolerance of salt stress) under salt stress as well [56,57]. At the same time, GCN5 was revealed to facilitate the acetylation of H3K9 and H3K14, which is associated with activation of HSFA3, UVH6, CTL1, PGX3, and MYB54 in Arabidopsis [56,57].…”

Histone acetylation orchestrates wound-induced transcriptional activation and cellular reprogramming in Arabidopsis

“…Blue arrows indicate the directionality of transcription. Line graphs display the transcriptional changes after wounding and error bars indicate the standard deviation (n = 3 independent experiments) dynamic than methylation 62 and it is involved in various stress and hormonal responses [63][64][65][66][67] . Our data therefore support the view that acetylation-mediated transcriptional modification is a general mechanism to swiftly respond to environmental or endogenous cues.…”